Glutamate increases pancreatic cancer cell invasion and migration via AMPA receptor activation and Kras-MAPK signaling

International Journal of Cancer

Volumn 129, Issue 10, 2011, Pages 2349-2359

  Herner, Alexander ^a   Sauliunaite, Danguole ^a   Michalski, Christoph W ^a   Erkan, Mert ^a   Oliveira, Tiago De ^a   Abiatari, Ivane ^a   Kong, Bo ^a   Esposito, Irene ^a   Friess, Helmut ^a   Kleeff, Jörg ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

AMPA; AMPA receptor; glutamate; pancreatic cancer

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; AMPA RECEPTOR; AMPA RECEPTOR ANTAGONIST; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR SUBUNIT 1; G PROTEIN COUPLED RECEPTOR SUBUNIT 2; G PROTEIN COUPLED RECEPTOR SUBUNIT 4; GLUTAMIC ACID; K RAS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN P42; PROTEIN P44; SMALL INTERFERING RNA; SYM 2206; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CANCER INVASION; CARCINOGENESIS; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME REPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PANCREATIC DUCTAL ADENOCARCINOMA; PANCREATIC INTRAEPITHELIAL NEOPLASIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ANIMALS; CARCINOMA, PANCREATIC DUCTAL; GLUTAMIC ACID; HUMANS; MICE; MICE, NUDE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; PANCREATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS; RAS PROTEINS; RECEPTORS, AMPA; SIGNAL TRANSDUCTION;

EID: 80052962633     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25898     Document Type: Article

References (45)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ,. Cancer statistics. CA Cancer J Clin 2008; 58: 71-96.
2. Esposito I, Seiler C, Bergmann F, Kleeff J, Friess H, Schirmacher P,. Hypothetical progression model of pancreatic cancer with origin in the centroacinar-acinar compartment. Pancreas 2007; 35: 212-7. (Pubitemid 47482512)
3. Hruban RH, Goggins M, Parsons J, Kern SE,. Progression model for pancreatic cancer. Clin Cancer Res 2000; 6: 2969-72. (Pubitemid 30637716)
4. Maitra A, Adsay NV, Argani P, Iacobuzio-Donahue C, De Marzo A, Cameron JL, Yeo CJ, Hruban RH,. Multicomponent analysis of the pancreatic adenocarcinoma progression model using a pancreatic intraepithelial neoplasia tissue microarray. Mod Pathol 2003; 16: 902-12. (Pubitemid 37152020)
5. Friess H, Ding J, Kleeff J, Fenkell L, Rosinski JA, Guweidhi A, Reidhaar-Olson JF, Korc M, Hammer J, Buchler MW,. Microarray-based identification of differentially expressed growth- and metastasis-associated genes in pancreatic cancer. Cell Mol Life Sci 2003; 60: 1180-99. (Pubitemid 36791920)
6. Friess H, Zhu Z, Liard V, Shi X, Shrikhande SV, Wang L, Lieb K, Korc M, Palma C, Zimmermann A, Reubi JC, Buchler MW,. Neurokinin-1 receptor expression and its potential effects on tumor growth in human pancreatic cancer. Lab Invest 2003; 83: 731-42. (Pubitemid 36618051)
7. Hartel M, di Mola FF, Selvaggi F, Mascetta G, Wente MN, Felix K, Giese NA, Hinz U, Di Sebastiano P, Buchler MW, Friess H,. Vanilloids in pancreatic cancer: potential for chemotherapy and pain management. Gut 2006; 55: 519-28.
8. Michalski CW, Maier M, Erkan M, Sauliunaite D, Bergmann F, Pacher P, Batkai S, Giese NA, Giese T, Friess H, Kleeff J,. Cannabinoids reduce markers of inflammation and fibrosis in pancreatic stellate cells. PLoS ONE 2008; 3: e1701.
9. Mijatovic T, Gailly P, Mathieu V, De Neve N, Yeaton P, Kiss R, Decaestecker C,. Neurotensin is a versatile modulator of in vitro human pancreatic ductal adenocarcinoma cell (PDAC) migration. Cell Oncol 2007; 29: 315-26. (Pubitemid 47037245)
10. Schuller HM, Al-Wadei HA, Majidi M,. GABA B receptor is a novel drug target for pancreatic cancer. Cancer 2008; 112: 767-78. (Pubitemid 351240570)
11. Takehara A, Hosokawa M, Eguchi H, Ohigashi H, Ishikawa O, Nakamura Y, Nakagawa H,. Gamma-aminobutyric acid (GABA) stimulates pancreatic cancer growth through overexpressing GABAA receptor pi subunit. Cancer Res 2007; 67: 9704-12. (Pubitemid 47621217)
12. Carracedo A, Gironella M, Lorente M, Garcia S, Guzman M, Velasco G, Iovanna JL,. Cannabinoids induce apoptosis of pancreatic tumor cells via endoplasmic reticulum stress-related genes. Cancer Res 2006; 66: 6748-55. (Pubitemid 44085633)
13. Fogli S, Nieri P, Chicca A, Adinolfi B, Mariotti V, Iacopetti P, Breschi MC, Pellegrini S,. Cannabinoid derivatives induce cell death in pancreatic MIA PaCa-2 cells via a receptor-independent mechanism. FEBS Lett 2006; 580: 1733-9.
14. Michalski CW, Laukert T, Sauliunaite D, Pacher P, Bergmann F, Agarwal N, Su Y, Giese T, Giese NA, Batkai S, Friess H, Kuner R,. Cannabinoids ameliorate pain and reduce disease pathology in cerulein-induced acute pancreatitis. Gastroenterology 2007; 132: 1968-78. (Pubitemid 46695719)
15. Michalski CW, Oti FE, Erkan M, Sauliunaite D, Bergmann F, Pacher P, Batkai S, Muller MW, Giese NA, Friess H, Kleeff J,. Cannabinoids in pancreatic cancer: correlation with survival and pain. Int J Cancer 2008; 122: 742-50.
16. Michalski CW, Shi X, Reiser C, Fachinger P, Zimmermann A, Buchler MW, Di Sebastiano P, Friess H,. Neurokinin-2 receptor levels correlate with intensity, frequency, and duration of pain in chronic pancreatitis. Ann Surg 2007; 246: 786-93. (Pubitemid 350035655)
17. Hollmann M, Heinemann S,. Cloned glutamate receptors. Annu Rev Neurosci 1994; 17: 31-108. (Pubitemid 24117025)
18. Kim CH, Lee J, Lee JY, Roche KW,. Metabotropic glutamate receptors: Phosphorylation and receptor signaling. J Neurosci Res 2007.
19. Rao VR, Finkbeiner S,. NMDA and AMPA receptors: old channels, new tricks. Trends Neurosci 2007; 30: 284-91. (Pubitemid 46802833)
20. Seeburg PH,. The TiPS/TINS lecture: the molecular biology of mammalian glutamate receptor channels. Trends Pharmacol Sci 1993; 14: 297-303. (Pubitemid 23242582)
21. Behar TN, Scott CA, Greene CL, Wen X, Smith SV, Maric D, Liu QY, Colton CA, Barker JL,. Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J Neurosci 1999; 19: 4449-61. (Pubitemid 29241096)
22. Ikonomidou C, Bosch F, Miksa M, Bittigau P, Vockler J, Dikranian K, Tenkova TI, Stefovska V, Turski L, Olney JW,. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 1999; 283: 70-4. (Pubitemid 29044848)
23. Joo JY, Kim BW, Lee JS, Park JY, Kim S, Yun YJ, Lee SH, Lee SH, Rhim H, Son H,. Activation of NMDA receptors increases proliferation and differentiation of hippocampal neural progenitor cells. J Cell Sci 2007; 120: 1358-70. (Pubitemid 46780029)
24. Komuro H, Rakic P,. Modulation of neuronal migration by NMDA receptors. Science 1993; 260: 95-7. (Pubitemid 23122752)
25. Hayashi T, Umemori H, Mishina M, Yamamoto T,. The AMPA receptor interacts with and signals through the protein tyrosine kinase Lyn. Nature 1999; 397: 72-6. (Pubitemid 29038251)
26. Ishiuchi S, Yoshida Y, Sugawara K, Aihara M, Ohtani T, Watanabe T, Saito N, Tsuzuki K, Okado H, Miwa A, Nakazato Y, Ozawa S,. Ca2+-permeable AMPA receptors regulate growth of human glioblastoma via Akt activation. J Neurosci 2007; 27: 7987-8001. (Pubitemid 47173326)
27. Stepulak A, Sifringer M, Rzeski W, Endesfelder S, Gratopp A, Pohl EE, Bittigau P, Felderhoff-Mueser U, Kaindl AM, Buhrer C, Hansen HH, Stryjecka-Zimmer M, et al. NMDA antagonist inhibits the extracellular signal-regulated kinase pathway and suppresses cancer growth. Proc Natl Acad Sci U S A 2005; 102: 15605-10. (Pubitemid 41528103)
28. Abdul M, Hoosein N,. N-methyl-D-aspartate receptor in human prostate cancer. J Membr Biol 2005; 205: 125-8. (Pubitemid 41803689)
29. Rzeski W, Turski L, Ikonomidou C,. Glutamate antagonists limit tumor growth. Proc Natl Acad Sci U S A 2001; 98: 6372-7. (Pubitemid 32488244)
30. Takeda M, Haga M, Yamada H, Kinoshita M, Otsuka M, Tsuboi S, Moriyama Y,. Ionotropic glutamate receptors expressed in human retinoblastoma Y79 cells. Neurosci Lett 2000; 294: 97-100.
31. Yoshioka A, Ikegaki N, Williams M, Pleasure D,. Expression of N-methyl-D-aspartate (NMDA) and non-NMDA glutamate receptor genes in neuroblastoma, medulloblastoma, and other cells lines. J Neurosci Res 1996; 46: 164-78.
32. Hauser R, Gos T, Krzyzanowski M, Goyke E,. The concentration of glutamate in cerebral tissue as a factor for the assessment of the emotional state before death. A preliminary report. Int J Legal Med 1999; 112: 184-7. (Pubitemid 29197590)
33. Erkan M, Kleeff J, Gorbachevski A, Reiser C, Mitkus T, Esposito I, Giese T, Buchler MW, Giese NA, Friess H,. Periostin creates a tumor-supportive microenvironment in the pancreas by sustaining fibrogenic stellate cell activity. Gastroenterology 2007; 132: 1447-64. (Pubitemid 46627568)
34. Reiser-Erkan C, Erkan M, Pan Z, Bekasi S, Giese NA, Streit S, Michalski CW, Friess H, Kleeff J,. Hypoxia-inducible proto-oncogene Pim-1 is a prognostic marker in pancreatic ductal adenocarcinoma. Cancer Biol Ther 2008; 7: 1352-9.
35. Hu H, Qin Y, Bochorishvili G, Zhu Y, van Aelst L, Zhu JJ,. Ras signaling mechanisms underlying impaired GluR1-dependent plasticity associated with fragile X syndrome. J Neurosci 2008; 28: 7847-62.
36. Zhu JJ, Qin Y, Zhao M, Van Aelst L, Malinow R,. Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 2002; 110: 443-55. (Pubitemid 35232288)
37. Qin Y, Zhu Y, Baumgart JP, Stornetta RL, Seidenman K, Mack V, van Aelst L, Zhu JJ,. State-dependent Ras signaling and AMPA receptor trafficking. Genes Dev 2005; 19: 2000-15. (Pubitemid 41247958)
38. Tian X, Feig LA,. Age-dependent participation of Ras-GRF proteins in coupling calcium-permeable AMPA glutamate receptors to Ras/Erk signaling in cortical neurons. J Biol Chem 2006; 281: 7578-82. (Pubitemid 43847528)
39. Ji B, Tsou L, Wang H, Gaiser S, Chang DZ, Daniluk J, Bi Y, Grote T, Longnecker DS, Logsdon CD,. Ras activity levels control the development of pancreatic diseases. Gastroenterology 2009; 137: 1072-82, 82 e1-6.
40. Carriere C, Young AL, Gunn JR, Longnecker DS, Korc M,. Acute pancreatitis markedly accelerates pancreatic cancer progression in mice expressing oncogenic Kras. Biochem Biophys Res Commun 2009; 382: 561-5.
41. Khasawneh J, Schulz MD, Walch A, Rozman J, Hrabe de Angelis M, Klingenspor M, Buck A, Schwaiger M, Saur D, Schmid RM, Kloppel G, Sipos B, et al. Inflammation and mitochondrial fatty acid beta-oxidation link obesity to early tumor promotion. Proc Natl Acad Sci U S A 2009; 106: 3354-9.
42. Strobel O, Dor Y, Alsina J, Stirman A, Lauwers G, Trainor A, Castillo CF, Warshaw AL, Thayer SP,. In vivo lineage tracing defines the role of acinar-to-ductal transdifferentiation in inflammatory ductal metaplasia. Gastroenterology 2007; 133: 1999-2009. (Pubitemid 350180811)
43. Guerra C, Schuhmacher AJ, Canamero M, Grippo PJ, Verdaguer L, Perez-Gallego L, Dubus P, Sandgren EP, Barbacid M,. Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice. Cancer Cell 2007; 11: 291-302. (Pubitemid 46349841)
44. Singh A, Greninger P, Rhodes D, Koopman L, Violette S, Bardeesy N, Settleman J,. A gene expression signature associated with "K-Ras addiction" reveals regulators of EMT and tumor cell survival. Cancer Cell 2009; 15: 489-500.
45. Ishiuchi S,. New roles of glutamate receptors in glias and gliomas. Brain Nerve 2009; 61: 753-64.